Same or Different: The Overlap Between Children With Auditory Processing Disorders and Children With Other Developmental Disorders: A Systematic Review

Abstract

Objectives: 

Children diagnosed with auditory processing disorders (APD) experience difficulties in auditory functioning and with memory, attention, language, and reading tasks. However, it is not clear whether the behavioral characteristics of these children are distinctive from the behavioral characteristics of children diagnosed with a different developmental disorder, such as specific language impairment (SLI), dyslexia, attention-deficit hyperactivity disorder (ADHD), learning disorder (LD), or autism spectrum disorder. This study describes the performance of children diagnosed with APD, SLI, dyslexia, ADHD, and LD to different outcome measurements. The aim of this study was to determine (1) which characteristics of APD overlap with the characteristics of children with SLI, dyslexia, ADHD, LD, or autism spectrum disorder; and (2) if there are characteristics that distinguish children diagnosed with APD from children diagnosed with other developmental disorders.

Design: 

A systematic review. Six electronic databases (Pubmed, CINAHL, Eric, PsychINFO, Communication & Mass Media Complete, and EMBASE) were searched to find peer-reviewed studies from 1954 to May 2015. The authors included studies reporting behaviors and performance of children with (suspected) APD and children diagnosed with a different developmental disorder (SLI, Dyslexia, ADHD, and LD). Two researchers identified and screened the studies independently. Methodological quality of the included studies was assessed with the American Speech-Language-Hearing Association’s levels-of-evidence scheme.

Results: 

In total, 13 studies of which the methodological quality was moderate were included in this systematic review. In five studies, the performance of children diagnosed with APD was compared with the performance of children diagnosed with SLI: in two with children diagnosed with dyslexia, one with children diagnosed with ADHD, and in another one with children diagnosed with LD. Ten of the studies included children who met the criteria for more than one diagnosis. In four studies, there was a comparison made between the performances of children with comorbid disorders. There were no studies found in which the performance of children diagnosed with APD was compared with the performance of children diagnosed with autism spectrum disorder. Children diagnosed with APD broadly share the same characteristics as children diagnosed with other developmental disorders, with only minor differences between them. Differences were determined with the auditory and visual Duration Pattern Test, the Children’s Auditory Processing Performance Scale questionnaire, and the subtests of the Listening in Spatialized Noise-Sentences test, in which noise is spatially separated from target sentences. However, these differences are not consistent between studies and are not found in comparison to all groups of children with other developmental disorders.

Conclusions: 

Children diagnosed with APD perform equally to children diagnosed with SLI, dyslexia, ADHD, and LD on tests of intelligence, memory or attention, and language tests. Only small differences between groups were found for sensory and perceptual functioning tasks (auditory and visual). In addition, children diagnosed with dyslexia performed poorer in reading tasks compared with children diagnosed with APD. The result is possibly confounded by poor quality of the research studies and the low quality of the used outcome measures. More research with higher scientific rigor is required to better understand the differences and similarities in children with various neurodevelopmental disorders.

INTRODUCTION

Children diagnosed with an auditory processing disorder (APD) have difficulty with listening. This is especially prominent in an unfavorable listening environment, despite well-functioning peripheral hearing (e.g., ^{American Academy of Audiology 2010; Geffner & Ross-Swain 2013}). Notwithstanding the attempts of special working groups to obtain clarification about the construct of APD (e.g., ^{American Speech-Language-Hearing Association 2005; American Academy of Audiology 2010; British Society of Audiology 2011}), discussion continues among professionals about the diagnostic criteria for APD, the overlap of APD with other developmental disorders, and whether APD exists as a unique diagnostic entity (^{Cacace & McFarland 2009; Moore et al. 2013; DeBonis 2015}).

Because of the lack of a clear definition and the use of multiple diagnostic criteria, different professionals approach children with listening complaints from different perspectives (^{McFarland & Cacace 2006}). Different diagnostic criteria for APD are proposed in various position statements and by several researchers (^{Bellis 2003; American Speech-Language-Hearing Association 2005; Dawes & Bishop 2009; McArthur 2009; American Academy of Audiology 2010; British Society of Audiology 2011; Wilson & Arnott 2013}). The different sets of diagnostic criteria have in common that children with listening difficulties are classified as having APD based on their performance on one or more behavioral central auditory tests or checklists or questionnaires. They differ, however, in the types of tests on which they must demonstrate inadequate performance and on how abnormal the performance is actually considered to be (e.g., <2 SD or <3 SD below the mean). The lack of a clear definition of APD together with the variation in diagnostic criteria for APD results in a range of approximate prevalence rates from 0.5% to 1.0% to 7% of the population (^{Chermak & Musiek 1997; Bamiou et al. 2001; Hind et al. 2011}). For instance, depending on which diagnostic criteria were used, ^{Wilson and Arnott (2013)} identified 7.3% (diagnostic criteria by ^{Bellis 2003}) to 96% (diagnostic criteria by ^{American Speech-Language-Hearing Association 2005}) of the children in their study group with APD.

Children with difficulties in the processing and understanding of auditory stimuli and with normal pure-tone thresholds have been recognized from the mid-20th century. These difficulties are “characterized by poor perception of both speech and non-speech” (^{British Society of Audiology 2011}, p. 3). Frequently reported symptoms are difficulty understanding speech in noisy environments; problems in locating the source of a signal; fail to response correctly to verbal information; frequently asking for repetition of information; reduced attention to auditory information, and easily distracted (^{American Academy of Audiology 2010}). Since the 1970s, these difficulties are more commonly known in the field of speech-language pathologists and audiologists as APD (^{American Speech-Language-Hearing Association 2005; Bellis 2007; Jerger 2009; Lucker 2013}). During recent years, this group of children is also described as children with suspected APD (susAPD) or children with listening difficulties.

One major issue that has dominated the field for many years concerns the distinction between APD and other developmental disorders, such as a specific language impairment (SLI), dyslexia, learning disorder (LD), attention-deficit hyperactivity disorder (ADHD), and autism spectrum disorders (ASD). The various developmental disorders have in common that they are characterized by developmental delays, which can cause impairment in personal, social, academic, or occupational functioning (^{American Psychiatric Association 2014}). Not all of the developmental disorders are well validated, and at the phenotypic level, the various developmental disorders overlap considerably with each other. Furthermore, research has shown that some disorders have in part the same genetic origin (^{Rutter & Pine 2015}). It is not clear whether there are different underlying mechanisms for the various disorders. Therefore, separation of the various developmental disorders from each other can be difficult for clinicians but also for scientific research (^{Rutter & Pine 2015}). This is also the case for APD. Several researchers have reported that the characteristics of children diagnosed with APD seem to correspond to the behaviors and symptoms of children diagnosed with other developmental disorders (^{Levy & Parkin 2003; Dawes & Bishop 2009; American Academy of Audiology 2010; British Society of Audiology 2011; Kamhi 2011; Miller 2011; Moore et al. 2013; DeBonis 2015}). For example, difficulties in comprehending and complying to verbal information are also commonly observed in children diagnosed with SLI. The concentration and attention complaints reported in children diagnosed with APD also correspond to the difficulties of children diagnosed with ADHD (^{Levy & Parkin 2003; Dawes & Bishop 2009}), and atypical processing of auditory information (e.g., difficulties listening in noise, hyperacusis, hypersensitivity to pitch), something that can be also difficult for children diagnosed with APD, is also an inherent component of ASD (^{Dawes & Bishop 2009; O’Connor 2012}). Likewise, it is contended that the diagnosis of a child may depend more on the referral route than on the symptoms of a child (^{Moore et al. 2013}).

The overlapping symptoms of children diagnosed with APD and children with other disorders also contribute to the discussion among clinicians and scientists as to whether APD can be considered a distinct clinical disorder (^{Levy & Parkin 2003; Cacace & McFarland 2009; Kamhi 2011; Medwetsky 2011; Moore et al. 2013}). One study indicated that 94% of the children identified with APD also had a comorbid language impairment or reading impairment (^{Sharma et al 2009}). In another study, 30% of the children with susAPD also had problems with reading and writing, 90% had additional speech–language problems, and 10% had ADHD. Sixty percent of the children had two or more accompanying problems (measured with a teacher-based questionnaire; ^{Neijenhuis et al. 2003}). Three possible explanations for the co-occurrence between APD and other developmental disorders are provided by ^{Moore et al. (2013)}: (1) not all different disorders can be distinguished from each other; the diagnosis of a child depends more on the reference route than by the symptoms; (2) SLI and dyslexia are caused by an APD; (3) a more general neurodevelopmental deficit is the cause of the various disorders.

Our recent systematic review (^{de Wit et al. 2016}) was aimed at establishing the characteristics of children with APD. The results showed that children with susAPD performed significantly poorer on tests of auditory processing when compared with typically developing (TD) children. However, significant differences between children with susAPD and TD children were not only found in the auditory domain. Children with susAPD also performed significantly poorer on tests of intelligence, memory, attention, and visual, language, and reading tests, as well as auditory brain measures. This again suggests that the characteristics of children diagnosed with APD overlap with the characteristics of children diagnosed with other developmental disorders. It is unclear whether a certain ensemble of symptoms exists that is solely attributable to difficulties with auditory processing. Such a distinctive symptom or group of symptoms could assist audiologists and speech–language pathologists in differentiating APD from other developmental disorders.

This present systematic review intends to describe the overlap between the characteristics of APD, SLI, dyslexia, ADHD, LD, and ASD. Our goal is to contribute to the discussion on whether APD is a distinct disorder that is separate from the other conditions that are mentioned. The central questions of this systematic review are the following: (1) Which characteristics of APD overlap with characteristics of other developmental disorders? and (2) Are there characteristics that distinguish children diagnosed with APD from children diagnosed with other developmental disorders?

MATERIALS AND METHODS

Studies published in peer-reviewed journals from 1954 to May 2015 were considered for inclusion in this systematic review. The four stages of the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) 2009 Flow Diagram (^{Moher et al. 2009}; prisma-statement.org) of (1) identification, (2) screening, (3) eligibility, and (4) inclusion were used for systematically going through the different phases of a systematic review. Stages 1 and 2, in which author 1, 4, and 7 of the current review were involved, are equal to those stages as described in the study of ^{de Wit et al. (2016)}.

After each stage, there was a consensus meeting held with the reviewers (author 1, 3, 4, and 7) who were involved in the process of assessing the studies that were found. A study was included or excluded in the subsequent stage when complete consensus was reached between reviewers.

Stage 1: Identification

To identify appropriate studies for this systematic review, the following databases were searched: Pubmed, CINAHL, Eric, PsychINFO, Communication & Mass Media Complete, and EMBASE. As described in ^{de Wit et al. (2016)}, the original search consisted of two separate search queries, which have been combined in this review to one search. Search strings used in the different databases are depicted in Table 1. The used search strategy can be found in Supplemental Digital Content 1, https://links.lww.com/EANDH/A355, which demonstrates the review protocol of this systematic review. RefWorks was used to manage, store, and share the found studies and for removing duplicates.

TABLE 1.: Search strings and databases used

Stage 2: Screening

The screening stage consisted of two steps, namely, (1) screening of titles and (2) screening of abstracts. For both steps in this stage, studies were screened against the inclusion and exclusion criteria by two researchers (author 1 and 4 or 1 and 7).

To be included in the review, the title and abstract of the study must meet the following criteria: (1) published in English and in a peer-reviewed journal; (2) addressed factors in title about auditory processing in combination with deficit(s), impairment(s), problem(s), difficulties, or disorder(s); (3) addressed elements in the abstract regarding the characteristics of susAPD or children at risk for APD in the presence of normal hearing. The terms/synonyms for APD that were also considered for inclusion can be found in Supplemental Digital Content 1, https://links.lww.com/EANDH/A355. In addition to these three inclusion criteria, studies must contain data regarding participants under the age of 18 years. The age limit of 18 years was chosen to search somewhat broader than the age at which the final step in structural maturation of the auditory cortex normally occurs (between the age of 6 and 12 years; ^{Moore & Linthicum 2007}). Studies that included neonates or participants with neuropathy, cochlear implants, Down syndrome or another syndrome, peripheral hearing loss, chronic otitis media, or brain damage were excluded from this review.

Stage 3: Eligibility

At the eligibility stage, it was decided which of the selected studies specifically matched the research question of the present study. Therefore, it was necessary that the focus of the study be on the comparison of the behaviors or performance of children with susAPD with children diagnosed with a different developmental disorder such as SLI, Dyslexia, ADHD, ASD, or LD. This stage consisted of two sequential steps: (1) full text articles assessed for eligibility and (2) full text articles assessed for methodological quality.

The full text of each identified study was individually evaluated by one of the three reviewers (author 1, 4, and 7). The reviewer assessed whether the study was appropriate for the topic of the current systematic review.

Subsequently, the methodological quality of each included study was independently reviewed by two reviewers (author 1 and 3 or 1 and 7) with the American Speech-Language-Hearing Association’s levels of evidence scheme (^{Mullen 2007}). A description of this quality assessment tool can be found in Supplemental Digital Content 1, https://links.lww.com/EANDH/A355 and Supplementary Table 1, https://links.lww.com/EANDH/A356. The quality indicator “intention-to-treat” was removed from the scheme. Each quality indicator that complied with the highest quality level was assigned one point (see Supplementary Table 1, https://links.lww.com/EANDH/A356). The maximum achievable quality score for a study was seven points.

To classify the evaluated studies, the final quality score of the individual studies was used (adapted to the quality assessment tool developed by ^{Gyorkos et al. 1994}). Based on their final quality score, studies were classified as strong (5–7 points), moderate (2–4 points), or weak (0–1 points). For inclusion in this systematic review, a study must have been appraised as a moderate or strong study. Studies rated as weak were excluded.

Stage 4: Inclusion

In stage 4, relevant data from the included studies with moderate and strong qualities were extracted and analyzed. The following data were extracted from the studies: (1) study characteristics; (2) subject characteristics; (3) measurement instruments; and (4) study results. Pooling the results of all of the studies was not possible because of the substantial variation in outcome measures and the inconsistent manner of presenting the results between studies. Therefore, the results of the individual studies are summarized in Tables 3–6. The overlap and differences between groups on the outcome of various measurements used in the included studies are summarized in a nonsymmetric Venn diagram (Fig. 2).

RESULTS

The result of stages 1 to 4 of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2009 flow diagram (^{Moher et al. 2009}) is illustrated in Figure 1. Database searching yielded 3317 unique studies (stage 1) of which the titles were screened independently by two reviewers. This yielded 548 studies of which the abstract was assessed (stage 2). Subsequently, three reviewers screened the eligibility of 194 full-text studies (stage 3). One hundred and eighty studies were excluded in this stage. Of these 180 studies, 53 studies matched the research question of the previously published systematic review, and 24 studies did not satisfy the research question of both reviews. In 70 studies, the auditory processing skills of children diagnosed with disorders other than APD were investigated. However, these studies were excluded because these studies are beyond the scope of our review and did not fit the research question and inclusion criteria of this review. Finally, 14 of the full-text studies were rated as appropriate for inclusion in the current systematic review (stage 4).

Fig. 1.: Process for identification of included studies. APD, auditory processing disorder. From PLoS Med. 2009;6:e1000097.

Methodological Quality of the Studies

Based on the total quality score, one study (^{Simões & Schochat 2010}) was classified as a study with weak quality (see Supplementary Table 2, https://links.lww.com/EANDH/A357 for details). Table 2 shows the methodological quality assessment of the included studies. As indicated in the data in Table 2, none of the studies were classified as being methodologically strong (≥5 points). In all of the included studies, significance and precision was either reported or could be calculated from the data; however, in none of the studies were the subjects randomly enrolled or subjects or assessors blinded.

TABLE 2.: Methodological quality of the included studies

General Study Characteristics

Thirteen studies are included in this systematic review. In one of the 13 studies, a comparison was made between children diagnosed with LD and children with APD + LD (^{Walker et al. 2011}) and, hence, not children diagnosed with only APD. In the other 12 studies, the performance of children diagnosed with APD was compared with the performance of children diagnosed with a different developmental disorder. In five studies, a comparison was made with children diagnosed with SLI (^{Ferguson et al. 2011; Miller & Wagstaff 2011; Rocha-Muniz et al. 2012,2014; Ferguson & Moore 2014}), two with children diagnosed with dyslexia (^{Dawes et al. 2009; Dawes & Bishop 2010}), one with children diagnosed with ADHD (^{Bellis et al 2011}), and another with children diagnosed with learning or attention disorders (LD group; ^{Cameron & Dillon 2008}). In three studies, a comparison was made between children diagnosed with APD and a group of children with comorbid disorders: two studies compared children diagnosed with APD with a group of children diagnosed with APD + ADHD (^{Riccio et al. 1994,1996}), and one compared children diagnosed with APD with a group of children diagnosed with APD + dyslexia (^{Iliadou et al. 2009}). No studies were found in which a comparison was made between the performance of children diagnosed with APD and children diagnosed with a disorder in the autistic spectrum.

In this systematic review, the diagnosis which primarily has been studied and was the focus of the original study was used in the comparison of the groups. It has been found that it is not always possible to fit children with developmental issues into stiff diagnosis categories. Ten of the studies included children who met the criteria for more than one diagnosis. In the studies of ^{Ferguson et al. (2011)} and ^{Ferguson and Moore (2014)}, more than 25% of the included children had an additional diagnosis of ADHD, ASD, or dyslexia. In the studies of ^{Dawes et al. (2009)} and ^{Dawes and Bishop (2010)}, these percentages were even higher: 52% of the children with a diagnosis of APD also met the diagnostic criteria of SLI, dyslexia, or both, and about 20% of the children in the dyslexia group also fits the diagnosis of SLI. In addition, there was also a high percentage of abnormal cases of hyperactivity and inattention in both groups. ^{Riccio et al. (1994,1996}) disclosed information about comorbid psychopathology (e.g., ADHD and conduct disorder). The authors also suspect coexisting language disorders because of low scores of the subjects on language tests and measures of cognitive ability. ^{Miller and Wagstaff (2011)} reported that the parents of 16 children indicated that there was also a diagnosis of attention-deficit disorders (ADD) or ADHD. There was no co-morbidity with ADHD or dysorthography in the subjects included in the study of ^{Iliadou et al. (2009)}; however, three children with low IQ and three children with borderline IQ were included. ^{Cameron and Dillon (2008)} and ^{Walker et al. (2011)} included children with LDs. This studies included children with different kinds of problems, like ADD, ADHD, SLI, dyslexia, and working memory deficits. In three studies, no information about additional diagnoses was given (^{Bellis et al. 2011; Rocha-Muniz et al. 2012,2014}).

Some participants took part in more than one study. In the study of ^{Ferguson and Moore (2014)} and ^{Dawes and Bishop (2010)}, participants were recruited from, respectively, the study of ^{Ferguson et al. (2011)} and ^{Dawes et al. (2009)}. For the study of ^{Rocha-Muniz et al. (2014)} and ^{Riccio et al. (1996)}, it is not clear whether the authors used partially the same participants as in the preceding studies (^{Riccio et al. 1994; Rocha-Muniz et al. 2012}). The number of subjects ranged from 7 to 41 in the APD group (mean = 20.8 subjects) and from 10 to 29 in the comparison group (the group of children included with a different developmental disorder: mean SLI = 23.8 subjects, mean dyslexia = 19 subjects, ADHD = 10 subjects, LD = 11 subjects, mean comorbid disorder = 13.5 subjects). The ages of the subjects in the APD group ranged from 6 years to 15 years and 11 months; in the SLI and dyslexia groups, from 6 to 13 years; in the LD group, from 7 years and 2 months to 11 years and 8 months; in the group with comorbid disorders, from 8 years to 15 years and 11 months; and in the ADHD group, the average age was 13 years and 1 month.

Diagnostic criteria for inclusion in the APD group varied among studies. Seven studies used the diagnostic criteria of a below normal performance on at least two behavioral diagnostic tests of auditory processing (^{Riccio et al. 1994; Iliadou et al. 2009; Bellis et al 2011; Miller & Wagstaff 2011; Walker et al. 2011; Rocha-Muniz et al. 2012,2014}), and three studies used a below normal performance on at least one behavioral diagnostic test of auditory processing (^{Riccio et al. 1996; Dawes et al. 2009; Dawes & Bishop 2010}). The remaining three studies used typically APD symptoms reported by parents or a referral for an auditory processing assessment for inclusion in the APD group (^{Cameron & Dillon 2008; Ferguson et al. 2011; Ferguson & Moore 2014}).

Five studies, which included an SLI group, used the diagnostic criteria of ^{Leonard (1998)}, referring to children with significant speech or language difficulties that could not be explained by factors such as hearing loss, autism, learning or physical disability, or bilingualism.

Participants in the studies that included children with ADHD met the diagnostic criteria from the Diagnostic and Statistical Manual of Mental Disorders (^{American Psychiatric Association 1980,1999}). In the two studies by Dawes, et al. (2009) and Dawes & Bishop (2010), the diagnosis of dyslexia was established by an educational psychologist in the event of a below normal performance (standard score <85) on a reading or spelling tests in the presence of an average intelligence (nonverbal IQ ≥80). ^{Iliadou et al. (2009)} used the Diagnostic and Statistical Manual of Mental Disorders-IV criteria for the diagnosis of dyslexia.

^{Cameron and Dillon (2008)} and ^{Walker et al. (2011)} used a very diverse patient population in their comparison group. The LD group in the study of ^{Cameron and Dillon (2008)} comprised children with various types of difficulties, such as working memory deficit, ADHD, and dyslexia. Also, the children in the LD group in the study of ^{Walker et al. (2011)} had various types of learning difficulties, including ADD, language and reading impairment, and more general learning impairments. All of the children in both studies had an overall intellectual performance within normal limits (^{Cameron & Dillon 2008}: a scaled score of eight or above, a standard score of 90 or above, or the equivalent percentile rank of 25 or above; ^{Walker et al. 2011}: full-scale IQ scores of 85 or greater).

Children Diagnosed With APD Versus Children Diagnosed With Other Developmental Disorders

Tables 3 to 6 show, per included study, a summary of the participant characteristics, measurement instruments used, and differences between children diagnosed with APD and children diagnosed with a different developmental disorder. It is apparent from this table that there were only marginal differences between these groups of children. Children diagnosed with SLI can be separated from children diagnosed with APD on the speech measures (weaker performance on the Children's Communication Checklist - second edition (CCC-2); subscale speech; speech-evoked auditory brain stem response; speech-in-noise test with monosyllabic words; and the Dichotic Digit test), and children diagnosed with dyslexia can be separated from children diagnosed with APD on the reading measures. On the contrary, children diagnosed with APD can be separated from children diagnosed with SLI and dyslexia on the listening questionnaire (Children’s Auditory Processing Performance Scale [CHAPPS] total score and subscales noise, multiple inputs, and attention). Opposed to children diagnosed with ADHD, children diagnosed with APD perform poorer on auditory and visual temporal ordering measures. Finally, children diagnosed with APD may be separated from children diagnosed with a variety of LDs by their problems with auditory stream segregation.

Five studies included different types of assessment of IQ, attention, and memory abilities in their study (^{Riccio et al. 1994,1996; Dawes & Bishop 2010; Ferguson et al. 2011; Miller & Wagstaff 2011}). No significant differences were found between clinical groups on one of these tests. Five studies examined the language and reading skills of children diagnosed with APD compared with children diagnosed with SLI, dyslexia, or ADHD (^{Riccio et al. 1994; Dawes & Bishop 2010; Ferguson et al. 2011; Miller & Wagstaff 2011; Walker et al. 2011}). Furthermore, all 13 studies assessed the auditory processing capabilities of the included children with auditory behavioral tests, speech-evoked auditory brain stem response, or parental/teacher questionnaires.

Children Diagnosed With APD Versus Children Diagnosed With SLI

Table 3 shows the similarities and differences on various measurement instruments between children diagnosed with APD and children diagnosed with SLI. No differences were found on IQ, working memory, language, and reading tests between children diagnosed with APD and children diagnosed with SLI. Most studies also found no difference between these children on behavioral auditory processing tests (^{Ferguson et al. 2011; Miller & Wagstaff 2011; Ferguson & Moore 2014}). Both groups experienced difficulties with speech perception. Two studies found comparably poorer performance for children with SLI in the perception of speech (^{Rocha-Muniz et al. 2012,2014}).The only study included in this systematic review that used electrophysiological measurements found that the children with SLI had a more impaired brainstem encoding for speech signals than the children with APD had (^{Rocha-Muniz et al. 2012}). Also, significance variances were found with the CHAPPS (^{Smoski et al. 1998}). Parents of children diagnosed with APD rated their children as having poorer listening skills in noisy places, poorer listening skills in multiple input, and poorer attention skills (^{Ferguson et al. 2011}).

TABLE 3.: Summary of the participant characteristics, reported measurements, and differences between children diagnosed with APD and children diagnosed with SLI

Children Diagnosed With APD Versus Children Diagnosed With Dyslexia

Table 4 shows the similarities and differences on various measurement instruments between children diagnosed with APD and children diagnosed with dyslexia. No differences were found on IQ, memory, and language tests between children diagnosed with APD and children diagnosed with dyslexia. Children in the dyslexia group performed poorer with reading abilities. Parents of children diagnosed with APD rated significantly more often that their child met characteristics for autism. Furthermore, the CHAPPS total score is worse in children diagnosed with APD (^{Dawes & Bishop 2010}). Children with comorbid APD and dyslexia performed significantly poorer on the duration pattern sequence test (^{Iliadou et al. 2009}).

TABLE 4.: Summary of the participant characteristics, reported measurements, and differences between children diagnosed with APD and children diagnosed with dyslexia

Children Diagnosed With APD Versus Children Diagnosed With ADHD

Table 5 shows the similarities and differences on various measurement instruments between children diagnosed with APD and children diagnosed with ADHD. No differences were found in performance on intelligence, attention, and language tests between children diagnosed with APD and children diagnosed with ADHD.

TABLE 5.: Summary of the participant characteristics, reported measurements, and differences between children diagnosed with APD and children diagnosed with ADHD

In two of the three included studies, there was, besides a group of children diagnosed with APD, a group of children with comorbid ADHD and APD included. Only one study included, besides a group of children diagnosed with APD, a group of children with a single diagnosis of ADHD. This one study found that the performance on the auditory and visual duration pattern test (DPT) can possibly distinguish children diagnosed with APD from children diagnosed with ADHD. Children with APD had significantly lower and divergent scores on the auditory and visual DPT (^{Bellis et al. 2011}).

Children Diagnosed With APD Versus Children Diagnosed With LD

Two studies compared the performance of children diagnosed with APD to the performance of children diagnosed with LD. Table 6 shows the similarities and differences on various measurement instruments between the children in these two groups.

TABLE 6.: Summary of the participant characteristics, reported measurements, and differences between children diagnosed with APD and children diagnosed with LD

The study of ^{Walker et al. (2011)} enrolled no group with children diagnosed with only APD in their study. No differences were found between these two groups on the auditory and visual temporal processing tasks and language and reading tests used in this studies. However, according to the authors, it is likely that the included group is very heterogeneous and contains children with ADD, language and reading problems, and more general developmental learning impairments (^{Walker et al. 2011}). Detailed information regarding the problems of these children is missing.

In the study of ^{Cameron and Dillon (2008)}, the performance on the Listening in Spatialized Noise-Sentences test (LiSN-S; ^{Cameron & Dillon 2007a}) of nine children with susAPD is compared with the performance of 11 children with various learning disabilities, such as ADHD, dyslexia, memory deficits, and visual processing problems. With the LiSN-S, the auditory stream segregation skills of a child—one specific part of listening—can be examined (^{Cameron & Dillon 2007b}). The test assesses if a child is capable to understand speech when noise is coming from different directions. ^{Cameron and Dillon (2008)} found that children with susAPD performed poorer in test conditions where the masker and target were spatially separated.

Overlap Between Groups on the Outcome of Various Tests

To be able to make a comparison between the performance of children diagnosed with APD and children diagnosed with other developmental disorders, the results of the isolated comparisons were analyzed and combined. Because comorbid groups can demonstrate additive effects of both disorders, only the studies in which children with APD were compared with children with a different developmental disorder were used for the overall comparison. Therefore, the four studies in which comorbid groups were enrolled were excluded for this analysis (^{Riccio et al. 1994,1996; Iliadou et al. 2009; Walker et al. 2011}). Figure 2 illustrates the pair-wise comparisons made in this systematic review and the overlap and differences on the outcomes of various tests used in the included studies for children diagnosed with APD and children diagnosed with SLI, dyslexia, ADHD, and LD. As mentioned earlier, also some children in the studies in which the focus was on the comparison of two different diagnostic groups have multiple diagnoses. This is not taken into account in this equation. The area of the circles is equal to the total number of subjects included in the studies in this analysis. The quantity N identifies the number of studies included (APD vs. SLI, N=5; APD vs. dyslexia, N=2; APD vs. ADHD, N=1; APD vs. LD, N=1). The amount n identifies the number of children included in the studies. All included children from the various studies are added together. This means that some children are counted twice because in a number of studies, the same participants took part in more than one study (e.g., ^{Dawes & Bishop 2010} and ^{Ferguson & Moore 2014}). No differences (bold and outlined numbers in Fig. 2) were found in the performance of children with APD compared with children with a different developmental disorder on the outcome of 85 of the 102 (sub)tests used in the included studies. Significantly poorer performance of children with APD (encircled italic numbers in Fig. 2) was found in the case of 10 (sub)tests (LiSN-S: high-cue speech reception threshold, spatial advantage and total advantage, ^{Cameron & Dillon 2008}; CHAPPS total score, ^{Dawes & Bishop 2010}; auditory and visual DPT, ^{Bellis et al. 2011}; CHAPPS total score and noise, multiple input and attention subscales, ^{Ferguson et al. 2011}). For seven (sub)tests, performances in children with SLI or dyslexia were poorer than in children with APD (literacy composite, ^{Dawes & Bishop 2010}; CCC-2 subscale speech, ^{Ferguson et al. 2011}; speech-evoked auditory brain stem response: timing-measure E and F peak and spectral encoding measure higher harmonics, ^{Rocha-Muniz et al. 2012}; speech-in-noise test and Dichotic digits test, ^{Rocha-Muniz et al. 2014}).

Fig. 2.: Venn diagram of the comparisons made in this systematic review and the overlap and differences between groups on the outcome of various tests used in the included studies. The performance of children diagnosed with APD on various tests is compared with the performance of children diagnosed with SLI, dyslexia, ADHD, and LD. N identifies the number of studies included. The area of the circles is equal to the number of subjects included in the studies (n). The bold and the outlined numbers show the overlap (no significant differences) on the oucome of the used measurement instruments. Italic numbers illustrate the significant differences between children diagnosed with APD and children diagnosed with other disorders. The encircled italic numbers show the number of measurement instruments (test and subtest level) whereupon children diagnosed with APD perform significantly poorer in comparison with children diagnosed with other developmental disorders. The studies in which children with comorbid disorders (N = 4) were enrolled are not captured in this figure. ADHD, attention-deficit hyperactivity disorder; APD, auditory processing disorder; CHAPPS, Children’s Auditory Processing Performance Scale (^{Smoski et al. 1998}); DPT, Duration Pattern test; LD, learning disorder; LiSN-S, Listening in Spatialized Noise test-Sentence (Cameron & Dillon 2007, ²⁰⁰⁸); SLI, specific language impairment; SRT, speech reception threshold.

DISCUSSION

The present study was designed (1) to determine which characteristics of APD overlap with the characteristics of SLI, dyslexia, ADHD, LD, and ASD and (2) to examine whether there are characteristics that distinguish children diagnosed with APD from children diagnosed with other developmental disorders. With respect to the first research question, we found that children diagnosed with APD and children diagnosed with SLI, dyslexia, ADHD, and LD have overlapping characteristics of intelligence, memory, attention, and language and that the reading skills of children diagnosed with APD overlap with the reading skills of children diagnosed with SLI. No studies were found in which the performance of children diagnosed with APD were compared with children diagnosed with ASD. Compared with TD children, children diagnosed with APD and children diagnosed with other disorders show broadly similar results. Unfortunately, not all studies reported how the performance on several tests of children in the research groups was compared to TD children (for details, see Tables 3–6. In the case of 57 (sub)tests (45.6%), both groups underperformed significantly compared with TD children or norm values, and in the case of 46 (sub)tests (36.8%), both groups displayed equal performance in comparison with TD children or norm values. With regard to the second research question, possible distinguishing characteristics for children diagnosed with APD were found in only four studies (^{Cameron & Dillon 2008; Dawes & Bishop 2010; Bellis et al. 2011; Ferguson et al. 2011}). ^{Ferguson et al. (2011)} compared the performance of 25 children diagnosed with APD to the performance of 22 children diagnosed with SLI. ^{Dawes and Bishop (2010)} also included 25 children diagnosed with APD and compared their performance to that of 19 children diagnosed with dyslexia. ^{Bellis et al. (2011)} included 7 children diagnosed with APD and 10 children with an ADHD diagnosis, and ^{Cameron and Dillon (2008)} compared the performance of 9 children diagnosed with APD to the performance of 11 children diagnosed with LD. These studies found that children with APD had (1) auditory and visual temporal ordering difficulties opposed to children diagnosed with ADHD, (2) poorer outcome on subtests of the LiSN-S compared to children diagnosed with LD, and (3) weaker listening skills opposed to children diagnosed with SLI and children diagnosed with dyslexia according to the parental evaluation. These characteristics may suggest a distinction between children diagnosed with APD and children diagnosed with SLI, dyslexia, ADHD, and LD. However, it is important to acknowledge that generalization to a broader population is limited because of the fact that these characteristics were found in single studies with small sample sizes, heterogeneous groups with comorbidity, and moderate methodological quality.

Overlap Between APD and SLI, Dyslexia, and ADHD

In this review, we found that children diagnosed with APD share overlapping intelligence, attention, memory, and language characteristics with children diagnosed with other developmental disorders. Executive functions could be a potentially useful construct for understanding the overlapping symptoms observed in different disorders, such as APD, ADHD, SLI, and dyslexia (^{Chermak et al. 1999; Thapar et al. 2015}). Executive functions appears to be related to the processing of language. Children diagnosed with SLI have demonstrated deficits in cognitive control related to deficits in language processing (^{Victorino & Schwartz 2015}). Such deficits are frequently incorporated into the general category of executive functions (^{Victorino & Schwartz 2015}). The overlapping symptoms of children diagnosed with APD, SLI, ADHD, and dyslexia fits the idea that it is difficult to say that the various psychiatric categories, as stated in the Diagnostic and Statistical Manual of Mental Disorders-V, are separate diagnosis with clear boundaries and a clear underlying cause. Our results support the idea that many of the individual categorical diagnoses are associated with each other in clusters, groups, or on a spectrum rather than that they are truly distinct disorders (^{Bishop & Snowling 2004; Pennington 2006; Bishop & Rutter 2008; Pennington & Bishop 2009; Moore & Hunter 2013; Bishop 2015; Vermiglio 2016}). A model that fits this idea is the multiple deficit model proposed by ^{Pennington (2006)}. The multiple deficit model assumes that a developmental disorder is caused by a combination of underlying specific and shared components (^{McGrath et al. 2011}). Pennington proposes with the model that, “the etiology of complex behavioral disorders is multifactorial and involves the interaction of multiple risk factors and protective factors, which can be either genetic or environmental” (^{Pennington 2006}, p. 404). As a result of the shared etiologic, comorbidity among neurodevelopmental disorders can be expected. Specific components ensure that the various developmental disorders differ slightly from each other on the surface. According to ^{Moore and Hunter (2013)}, the various psychiatric categories can be conceptualized as a more general neurodevelopmental syndrome, wherein the behavioral difficulties (e.g., auditory, language, and attentional) of children serve as markers that can be expressed along a continuum of severity (^{Wallach 2011; Moore et al. 2013; Moore & Hunter 2013}).

Differences Between APD and SLI, Dyslexia, and ADHD

The APD group demonstrated significantly lower performance on the CHAPPS questionnaire (^{Dawes & Bishop 2010; Ferguson et al. 2011}) and the subtests of the LiSN-S in which the noise was spatially separated from the target speech (^{Cameron & Dillon 2008}). This may indicate that difficulties with the ability to listen in noisy conditions in challenging environments is a distinctive characteristic for children with susAPD. Difficulties in noisy environments are one of the most mentioned symptoms of children with susAPD (^{Jerger & Musiek 2000; American Speech-Language-Hearing Association 2005}). However, there are a number of concerns regarding the interpretation of the experimental evidence that children diagnosed with APD experience “difficulties with listening in noise.”

Information regarding the validity and reliability of the CHAPPS questionnaire (^{Smoski et al. 1998}) is lacking, whereby it is not certain what is actually measured (^{American Academy of Audiology 2010; Moore et al. 2013; Barry et al. 2015}). A number of studies have examined the clinical utility of the CHAPPS (^{Lam & Sanchez 2007; Wilson et al. 2011; Iliadou & Bamiou 2012; Ahmmed & Ahmmed 2016}). Hereby, varying results are reported. ^{Lam and Sanchez (2007)} and ^{Wilson et al. (2011)} found that the CHAPPS has no significant predictive capability for APD, while others (^{Iliadou & Bamiou 2012; Ahmmed & Ahmmed 2016}) reported that a number of subsections (Listening condition: ideal, auditory memory/sequencing, and auditory attention span) of the CHAPPS may be clinically useful for identifying listening difficulties in children; however, further research is needed. The CHAPPS is originally designed to be completed by the teacher of the child (^{Smoski et al. 1992}). The teacher answers the questions by comparing the listening skills of the individual child with the listening skills of other children of the same age group and background (^{Smoski et al. 1998}). However, in both studies included in this systematic review, the CHAPPS was completed by parents instead of the teacher. This may plausibly cause a referral bias because parents of children with a diagnosis of APD could complete the questionnaire from a different perspective than parents of children with a diagnosis of SLI or dyslexia (^{Ferguson et al. 2011}). No clear relationship between CHAPPS scores and the diagnosis APD were found in studies in which the CHAPPS questionnaire was completed by the child’s teacher (^{Lam & Sanchez 2007; Wilson et al. 2011}).

The results of this systematic review suggest that the LiSN-S (^{Cameron & Dillon 2007a}) could perhaps be a valuable instrument to differentiate between children diagnosed with APD and children diagnosed with other developmental disorders. The LiSN-S was designed to assess auditory stream segregation skills in children with susAPD (^{Cameron & Dillon 2007b}) and can be used to examine spatial processing difficulties (^{Chermak et al. 2017}). With this test, one specific part of the whole range of listening abilities children need to have to be able to pick up information from what they hear can be examined. The LiSN-S has a high test–retest reliability, and normative data are provided for people aged 6 to 60 years (^{Cameron & Dillon 2007b; Cameron et al. 2009,2011}). However, the LiSN-S is only used in one of the 14 included studies. In addition, the study group of this one study was very small (9 children diagnosed with APD versus 11 children diagnosed with learning or attention disorders). Studies that previously have used the LiSN-S to examine the differences between children with susAPD and TD children found varying results. Cameron and Dillon (^{Cameron et al. 2006; Cameron & Dillon 2008}) found that the inability to use spatial information may be one important cause of the listening difficulties in children. Others found no differences in spatial processing between children with susAPD and TD children on the LiSN-S Test (^{Sharma et al. 2014; Barry et al. 2015}). As also explained by the authors themselves, it would be beneficial to conduct studies that are more large scale in the future with the LiSN-S to investigate whether the test can be used to distinguish between children with and without spatial processing difficulties.

The significant underperformance of children diagnosed with APD on the auditory and visual DPT in the study of ^{Bellis et al. (2011)} indicates that a nonmodal-specific temporal ordering deficit may also be a possible characteristic that distinguish children diagnosed with APD from children diagnosed with other developmental disorders. ^{Bellis et al. (2011)} used an auditory DPT (^{Pinheiro & Musiek 1985; Musiek et al. 1990}) in their study with triads of 1000 Hz tone bursts differing in short (250 msec) and long (500 msec) duration. For the auditory DPT (^{Musiek 1994}), the levels of diagnostic accuracy (sensitivity, 0.86; specificity, 0.92) are known (^{Friberg & McNamara 2010; Vermiglio 2016}). The visual DPT (self-developed) consisted of a black rectangle presented on a white screen in short (250 msec) and long (800 msec) triads. ^{Bellis et al. (2011)} reported robust effect sizes despite the small number of participants. The differences between children diagnosed with APD and children diagnosed with ADHD in auditory and visual DPT suggest that the deficits of children with listening difficulties are not specific to the auditory modality because children diagnosed with APD underperformed on both the visual and auditory version. Some authors proposed that problems in auditory processing are modality-specific if the problems are only situated in the auditory modality (^{Cacace & McFarland 2005,2013}). When there are also problems in other modalities, such as problems with visual tasks, they would rather not speak of APD. Furthermore, there is no evidence that the DPT also differentiates between children diagnosed with APD and children diagnosed with SLI or dyslexia. In the study of ^{Iliadou et al. (2009)}, children with a diagnosis of APD and dyslexia scored poorer on the DPT compared with children with a diagnosis of only APD. Also, no differences between children diagnosed with APD and children diagnosed with SLI in performance on the DPT were found by ^{Miller and Wagstaff (2011)}. Studies in which auditory pattern recognition is examined found similar results, that is, children diagnosed with dyslexia or SLI perform poorer than TD children in the detection of duration patterns (^{Walker et al. 2002; King et al. 2003; Stollman et al. 2003; Walker et al. 2006}). Therefore, it cannot be argued that a temporal ordering deficit is a distinguishing characteristic for APD.

In general, there is substantial overlap between children with various developmental disorders. The performance of children diagnosed with APD on three outcome measurements (CHAPPS, LiSN-S, and DPT) suggested that there are differences between children diagnosed with APD and children diagnosed with other developmental disorders. However, the results are not consistent and the findings seem insufficiently researched; hence, it remains ambiguous whether these results are replicable. As previously mentioned by ^{Moore and Hunter (2013)}, the various developmental disorders could be conceptualized as a general neurodevelopmental syndrome wherein “auditory, speech, language, attention, memory and behavioral difficulties (markers) in children are expressed along a continuum of severity” (^{Moore & Hunter 2013}, pp. 165). Perhaps, it is possible to use the three outcome measurements found in this review to indicate where children are located on this continuum.

Methodological Quality

All included studies in this systematic review had moderate methodological quality because none of the studies used a random sample, because none of the assessors were blinded, and because it was not clear if the participants in the different groups were comparable or not at baseline. In most studies, it was also not evident whether the children in the various groups (APD, SLI, ADHD, and dyslexia) had additional deficits besides the primary diagnosis they had received. The studies did not describe a broad assessment at the beginning to (1) check the specified diagnosis and (2) investigate all important skills covering all developmental areas. It could be that the number of pure cases of children with APD, SLI, ADHD, or dyslexia is negligible if a detailed assessment battery was used at the beginning of the studies (^{Bishop & Rutter 2008}). The absence of valid auditory processing measurement instruments is another factor that is of influence on the methodological quality of the studies. There are no valid auditory processing tests available because there is no reference standard for the assessment of APD (^{Vermiglio 2016}).

Clinical Implications and Future Research

Children with various developmental disorders perform similar on the outcome of 85 of the 102 (sub)tests (see Tables 3–6 and Fig. 2 for details). No significant differences were found between groups on most auditory tests and on questionnaires and tests of intelligence, attention, memory, language, and reading. With the current measurement instruments used in clinical practice, it is difficult to distinguish the various disorders from each other. From the results of our previous systematic review (^{de Wit et al. 2016}), we know that children with susAPD perform significantly lower, compared to TD children, on auditory behavioral tests. Clinicians should take into account the fact that if children have abnormal performance on a test for auditory processing, this does not automatically signify that the child has APD. Otherwise stated, the tests may distinguish abnormal from normal performance; however, they are not able to distinguish the various conditions from each other. It is also known that failure on a specific test not necessarily mean that the child has a problem (^{Dillon et al. 2012}). Also TD children show considerable variability on at least some of these measures. From this and our previous review (^{de Wit et al. 2016}), it is evident that listening difficulties experienced by children are multifaceted and that there is substantial overlap between various developmental disorders. As ^{Moore (2016)} stated, “Hearing necessarily involves the ear, the central auditory nervous system, and other brain systems, including attention, memory and vision.” Therefore, it is crucial that various professions work together and use a multidisciplinary approach not only in the assessment of children with listening complaints but also in the event of children who satisfy the diagnostic standards of SLI, ADHD, and dyslexia. This accords with the latest suggestion of ^{Chermak et al. (2017)} who stated that an audiologist, speech–language pathologist, and psychologist must collectively decide whether the listening difficulties arise from an auditory issue, problems with processing language, cognitive deficiencies such as attention, executive function, or working memory, or an aggregation of them. It is important to note that the similarities found in this systematic review between children with various disorders are valid on a group level and does not reveal individual differences. Audiologists, speech–language pathologists, and psychologists should focus on the performance of the individual child. To apply appropriate treatment, the symptoms and complaints in everyday life of the individual child must be focused on and not necessarily the diagnostic label.

The findings across the 13 studies should be interpreted according to study quality and design characteristics. Heterogeneity of the participants, inadequate reporting of the profile of participants, large variability in the measures and procedures used across studies, and a minimal number of studies with sometimes a small sample size should be taken into account when making comparisons between studies. There is a clear need for higher quality, well-designed studies in which a comparison is made between different groups of children with various disorders. We recommend that these studies include multiple groups of children with different diagnoses and the use of a detailed assessment battery incorporating the entire range of symptoms of neurodevelopmental disorders so that not only the performance of children diagnosed with APD is compared to the performance of children diagnosed with some other disorder but that the performance of children with all various developmental disorders can be compared with each other and that the entire continuum of developmental disorders can be identified.

Limitations of the Current Review

The limitations of this systematic review are the same as the restrictions listed in our previous study (^{de Wit et al. 2016}), specifically (1) only articles written in English were included; (2) case studies were excluded; (3) studies in which auditory processing or one of the used synonyms was not mentioned in the title were excluded; and (4) another way of classifying the methodological quality of the studies could lead to other studies included or excluded in this review. Unfortunately, conducting a meta-analysis was not possible because of the diversity among outcome measures and the wide variation in the descriptive of participants.

CONCLUSION

Only marginal differences were found between children diagnosed with APD and children diagnosed with a different developmental disorder. Children diagnosed with APD and children diagnosed with SLI, dyslexia, ADHD, and LD have overlapping characteristics in terms of intelligence, memory, attention, and language. The reading skills of children diagnosed with APD overlap with the reading skills of children diagnosed with SLI. The results suggest that the CHAPPS questionnaire and the subtests of the LiSN-S in which noise is spatially separated from target sentences could possibly differentiate between children with difficulties in auditory functioning and children with language, reading, and attention disorders. However, this result is possibly confounded by the generally poor quality of the research studies included in this review and the quality of the used outcome measures. Additional research is required to better understand the different profiles of children with various complaints or disorders.

ACKNOWLEDGMENTS

This research was funded by the Netherlands Organisation for Scientific Research (NWO).

Preliminary results of this study were presented by poster presentation on the British Society of Audiology Annual Conference 2016 and by oral presentation on the 30th World Congress of the International Association of Logopedics and Phoniatrics (I.A.L.P.) 2016.